Novel Striatal GABAergic Interneuron Populations Labeled in the 5HT3aEGFP Mouse

Cerebral Cortex

Volumn 26, Issue 1, 2016, Pages 96-105

  Munoz Manchado A B ^a   Foldi, C ^a   Szydlowski, S ^a   Sjulson, L ^b   Farries, M ^c   Wilson, C ^c   Silberberg, G ^a   Hjerling Leffler, J ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

5HT3a; interneuron; nicotine; striatum; subtype

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; NEUROPEPTIDE Y; NICOTINE; NITRIC OXIDE SYNTHASE; PARVALBUMIN; SEROTONIN 3A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; GREEN FLUORESCENT PROTEIN; SEROTONIN TRANSPORTER; SOMATOSTATIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CELL LABELING; CELL POPULATION; CELL STRUCTURE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CORPUS STRIATUM; DORSOLATERAL STRIATUM; ELECTROPHYSIOLOGICAL PROCEDURES; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; IMMUNOHISTOCHEMISTRY; INTERNEURON; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ACTION POTENTIAL; ANIMAL; CYTOLOGY; ELECTROSTIMULATION; METABOLISM; NEOSTRIATUM; NERVE TRACT; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CORPUS STRIATUM; ELECTRIC STIMULATION; GABAERGIC NEURONS; GREEN FLUORESCENT PROTEINS; INTERNEURONS; NEOSTRIATUM; NEURAL PATHWAYS; NEUROPEPTIDE Y; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SOMATOSTATIN;

EID: 84952936868     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu179     Document Type: Article

References (46)

1. Arlotta P, Molyneaux BJ, Jabaudon D, Yoshida Y, Macklis JD. 2008. Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J Neurosci. 28(3): 622-632.
2. Baraban SC, Hollopeter G, Erickson JC, Schwartzkroin PA, Palmiter RD. 1997. Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J Neurosci. 17(23): 8927-8936.
3. Blandina P, Goldfarb J, Craddock-Royal B, Green JP. 1989. Release of endogenous dopamine by stimulation of 5-hydroxytryptamine3 receptors in rat striatum. J Pharmacol Exp Ther. 251(3): 803-809.
4. Bolam JP, Clarke DJ, Smith AD, Somogyi P. 1983. A type of aspiny neuron in the rat neostriatum accumulates [3H]gamma-aminobutyric acid: combination of Golgi-staining, autoradiography, and electron microscopy. J Comp Neurol. 213(2): 121-134.
5. Chittajallu R, Craig MT, McFarland A, Yuan X, Gerfen S, Tricoire L, Erkkila B, Barron SC, Lopez CM, Liang BJ et al. 2013. Dual origins of functionally distinct O-LM interneurons revealed by differential 5-HT3AR expression. Nat Neurosci. 16(11): 1598-1607.
6. Cobos I, Long JE, Thwin MT, Rubenstein JL. 2006. Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb Cortex. 16 (Suppl 1): i82-i88.
7. Darmopil S, Muneton-Gomez VC, de Ceballos ML, Bernson M, Moratalla R. 2008. Tyrosine hydroxylase cells appearing in the mouse striatum after dopamine denervation are likely to be projection neurones regulated by L-DOPA. Eur J Neurosci. 27(3): 580-592.
8. Deacon TW, Pakzaban P, Isacson O. 1994. The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: neural transplantation and developmental evidence. Brain Res. 668(1-2): 211-219.
9. English DF, Ibanez-Sandoval O, Stark E, Tecuapetla F, Buzsaki G, Deisseroth K, Tepper JM, Koos T. 2012. GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci. 15(1): 123-130.
10. Fishell G, Rudy B. 2011. Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu Rev Neurosci. 34: 535-567.
11. Fragkouli A, van Wijk NV, Lopes R, Kessaris N, Pachnis V. 2009. LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development. 136(22): 3841-3851.
12. Franklin KBJ, Paxinos G. 2008. The mouse brain in stereotaxic coordinates. 3rd ed. Amsterdam: Elsevier.
13. Gerfen CR, Wilson CJ. 1996. Chapter II: The basal ganglia. In: Swanson LW, Björklund A, Hökfelt T, editors. Handbook of chemical neuroanatomy. Vol. 12: integrated systems of the CNS, part III. Amsterdam: Elsevier. p. 371-468.
14. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC. 2010. Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J Neurosci. 30(6): 2223-2234.
15. Graveland GA, DiFiglia M. 1985. The frequency and distribution of medium-sized neurons with indented nuclei in the primate and rodent neostriatum. Brain Res. 327(1-2): 307-311.
16. Hanna MC, Davies PA, Hales TG, Kirkness EF. 2000. Evidence for expression of heteromeric serotonin 5-HT(3) receptors in rodents. J Neurochem. 75(1): 240-247.
17. Herbison AE, Simonian SX, Norris PJ, Emson PC. 1996. Relationship of neuronal nitric oxide synthase immunoreactivity to GnRH neurons in the ovariectomized and intact female rat. J Neuroendocrinol. 8(1): 73-82.
18. Horner KA, Westwood SC, Hanson GR, Keefe KA. 2006. Multiple high doses of methamphetamine increase the number of preproneuropeptide Y mRNA-expressing neurons in the striatum of rat via a dopamine D1 receptor-dependent mechanism. J Pharmacol Exp Ther. 319(1): 414-421.
19. Ibanez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koos T, Tepper JM. 2010. Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum. J Neurosci. 30(20): 6999-7016.
20. Ibanez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koos T, Tepper JM. 2011. A novel functionally distinct subtype of striatal neuropeptide Y interneuron. J Neurosci. 31(46): 16757-16769.
21. Iversen LL, Schon FE. 1973. The use of autoradiographic techniques for the identification and mapping of transmitter-specific neurons in the CNS. In: Mandell AJ, editor. New concepts in neurotransmitter regulation. New York: Plenum Press. p. 153-193.
22. Jollivet C, Montero-Menei CN, Venier-Julienne MC, Sapin A, Benoit JP, Menei P. 2004. Striatal tyrosine hydroxylase immunoreactive neurons are induced by L-dihydroxyphenylalanine and nerve growth factor treatment in 6-hydroxydopamine lesioned rats. Neurosci Lett. 362 (2): 79-82.
23. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC. 1995. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 18(12): 527-535.
24. Kita H. 1993. GABAergic circuits of the striatum. Prog Brain Res. 99: 51-72.
25. Kita H, Kitai ST. 1988. Glutamate decarboxylase immunoreactive neurons in rat neostriatum: Their morphological types and populations. Brain Res. 447(2): 346-352.
26. Koos T, Tepper JM. 1999. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci. 2(5): 467-472.
27. Koos T, Tepper JM. 2002. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci. 22(2): 529-535.
28. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. 2010. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci. 30(50): 16796-16808.
29. Lindefors N, Brene S, Herrera-MarschitzM, Persson H. 1989. Region specific regulation of glutamic acid decarboxylase mRNA expression by dopamine neurons in rat brain. Exp Brain Res. 77(3): 611-620.
30. Luk KC, Sadikot AF. 2001. GABA promotes survival but not proliferation of parvalbumin-immunoreactive interneurons in rodent neostriatum: An in vivo study with stereology. Neuroscience. 104(1): 93-103.
31. Maricq AV, Peterson AS, Brake AJ, Myers RM, Julius D. 1991. Primary structure and functional expression of the 5HT3 receptor, a serotonin-gated ion channel. Science. 254(5030): 432-437.
32. Morales M, Wang SD. 2002. Differential composition of 5-hydroxytryptamine3 receptors synthesized in the rat CNS and peripheral nervous system. J Neurosci. 22(15): 6732-6741.
33. Nery S, Fishell G, Corbin JG. 2002. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci. 5(12): 1279-1287.
34. Oorschot DE. 2013. The percentage of interneurons in the dorsal striatum of the rat, cat, monkey and human: A critique of the evidence. Basal Ganglia. 3(1): 19-24.
35. Phelps PE, Houser CR, Vaughn JE. 1985. Immunocytochemical localization of choline acetyltransferase within the rat neostriatum: A correlated light and electron microscopic study of cholinergic neurons and synapses. J Comp Neurol. 238(3): 286-307.
36. Rubin AN, Alfonsi F, Humphreys MP, Choi CK, Rocha SF, Kessaris N. 2010. The germinal zones of the basal ganglia but not the septum generate GABAergic interneurons for the cortex. J Neurosci. 30 (36): 12050-12062.
37. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol. 71(1): 45-61.
38. Rymar VV, Sasseville R, Luk KC, Sadikot AF. 2004. Neurogenesis and stereological morphometry of calretinin-immunoreactive GABAergic interneurons of the neostriatum. J Comp Neurol. 469 (3): 325-339.
39. Sullivan MA, Chen H, Morikawa H. 2008. Recurrent inhibitory network among striatal cholinergic interneurons. J Neurosci. 28 (35): 8682-8690.
40. Szydlowski SN, Pollak Dorocic I, Planert H, Carlen M, Meletis K, Silberberg G. 2013. Target selectivity of feedforward inhibition by striatal fast-spiking interneurons. J Neurosci. 33(4): 1678-1683.
41. Tepper JM, Tecuapetla F, Koos T, Ibanez-Sandoval O. 2010. Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat. 4: 150.
42. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ. 2012. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron. 75(1): 58-64.
43. Tricoire L, Pelkey KA, Erkkila BE, Jeffries BW, Yuan X, McBain CJ. 2011. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci. 31(30): 10948-10970.
44. Vuillet J, Kerkerian-Le Goff L, Kachidian P, Dusticier G, Bosler O, Nieoullon A. 1990. Striatal NPY-containing neurons receive GABAergic afferents and may also contain GABA: An electron microscopic study in the rat. Eur J Neurosci. 2(8): 672-681.
45. Wirth MJ, Obst K, Wahle P. 1998. NT-4/5 and LIF, but not NT-3 and BDNF, promote NPY mRNA expression in cortical neurons in the absence of spontaneous bioelectrical activity. Eur J Neurosci. 10 (4): 1457-1464.
46. Xu Q, Tam M, Anderson SA. 2008. Fate mapping Nkx2. 1-lineage cells in the mouse telencephalon. J Comp Neurol. 506(1): 16-29.